How coral reefs survive as oases of life in low-productivity oceans has puzzled scientists for centuries. The answer may lie in internal nutrient cycling and/or input from the pelagic zone. Integrating meta-analysis, field data, and population modeling, we show that the ocean’s smallest vertebrates, cryptobenthic reef fishes, promote internal reef fish biomass production through extensive larval supply from the pelagic environment. Specifically, cryptobenthics account for two-thirds of reef fish larvae in the near-reef pelagic zone despite limited adult reproductive outputs. This overwhelming abundance of cryptobenthic larvae fuels reef trophodynamics via rapid growth and extreme mortality, producing almost 60% of consumed reef fish biomass. Although cryptobenthics are often overlooked, their distinctive demographic dynamics may make them a cornerstone of ecosystem functioning on modern coral reefs.